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Evolutionary insights about bacterial GlxRS from whole genome analyses: is GluRS2 a chimera?

Dasgupta S, Basu G - BMC Evol. Biol. (2014)

Bottom Line: Non-functional GluRS2 (as in Thermotoga maritima), on the other hand, was found to contain an anticodon-binding domain appended to a gene-duplicated catalytic domain.Several genomes were found to possess both GluRS2 and GlnRS, even though they share the common function of aminoacylating tRNAGln.The functional annotation of GluRS, without recourse to experiments, performed in this work, demonstrates the inherent and unique advantages of using whole genome over isolated sequence databases.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biophysics, Bose Institute, P-1/12 CIT Scheme VIIM, Kolkata 700054, India. gautam@boseinst.ernet.in.

ABSTRACT

Background: Evolutionary histories of glutamyl-tRNA synthetase (GluRS) and glutaminyl-tRNA synthetase (GlnRS) in bacteria are convoluted. After the divergence of eubacteria and eukarya, bacterial GluRS glutamylated both tRNAGln and tRNAGlu until GlnRS appeared by horizontal gene transfer (HGT) from eukaryotes or a duplicate copy of GluRS (GluRS2) that only glutamylates tRNAGln appeared. The current understanding is based on limited sequence data and not always compatible with available experimental results. In particular, the origin of GluRS2 is poorly understood.

Results: A large database of bacterial GluRS, GlnRS, tRNAGln and the trimeric aminoacyl-tRNA-dependent amidotransferase (gatCAB), constructed from whole genomes by functionally annotating and classifying these enzymes according to their mutual presence and absence in the genome, was analyzed. Phylogenetic analyses showed that the catalytic and the anticodon-binding domains of functional GluRS2 (as in Helicobacter pylori) were independently acquired from evolutionarily distant hosts by HGT. Non-functional GluRS2 (as in Thermotoga maritima), on the other hand, was found to contain an anticodon-binding domain appended to a gene-duplicated catalytic domain. Several genomes were found to possess both GluRS2 and GlnRS, even though they share the common function of aminoacylating tRNAGln. GlnRS was widely distributed among bacterial phyla and although phylogenetic analyses confirmed the origin of most bacterial GlnRS to be through a single HGT from eukarya, many GlnRS sequences also appeared with evolutionarily distant phyla in phylogenetic tree. A GlnRS pseudogene could be identified in Sorangium cellulosum.

Conclusions: Our analysis broadens the current understanding of bacterial GlxRS evolution and highlights the idiosyncratic evolution of GluRS2. Specifically we show that: i) GluRS2 is a chimera of mismatching catalytic and anticodon-binding domains, ii) the appearance of GlnRS and GluRS2 in a single bacterial genome indicating that the evolutionary histories of the two enzymes are distinct, iii) GlnRS is more widespread in bacteria than is believed, iv) bacterial GlnRS appeared both by HGT from eukarya and intra-bacterial HGT, v) presence of GlnRS pseudogene shows that many bacteria could not retain the newly acquired eukaryal GlnRS. The functional annotation of GluRS, without recourse to experiments, performed in this work, demonstrates the inherent and unique advantages of using whole genome over isolated sequence databases.

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Phylogeny of bacterial GluRS1 and GluRS2. Phylogenetic tree of bacterial GluRS1 and GluRS2 sequences (listed in Additional file 5) and annotated with bacterial phyla (abbreviations in Table 1). Experimentally determined glutamylation capacity of both GluRS1 and GluRS2 for selected bacterial species (H. pylori, A. ferrooxidans and T. maritima) with the two isoacceptors of tRNAGlu (E1: 34UUC and E2: 34CUC) and tRNAGln (Q1: 34UUG and Q2: 34CUG), are projected in the respective clades, as productive or non-productive (empty/filled symbols). Branch support values < 0.7, calculated using aLRT statistics, are indicated.
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Figure 5: Phylogeny of bacterial GluRS1 and GluRS2. Phylogenetic tree of bacterial GluRS1 and GluRS2 sequences (listed in Additional file 5) and annotated with bacterial phyla (abbreviations in Table 1). Experimentally determined glutamylation capacity of both GluRS1 and GluRS2 for selected bacterial species (H. pylori, A. ferrooxidans and T. maritima) with the two isoacceptors of tRNAGlu (E1: 34UUC and E2: 34CUC) and tRNAGln (Q1: 34UUG and Q2: 34CUG), are projected in the respective clades, as productive or non-productive (empty/filled symbols). Branch support values < 0.7, calculated using aLRT statistics, are indicated.

Mentions: In order to further probe the evolutionary relationship between GluRS1 and GluRS2, a phylogenetic tree was constructed, exclusively with GluRS1 and GluRS2 sequences (Additional file 5). The GluRS1/GluRS2 phylogeny (Figure 5) shows a clear division between GluRS1 and GluRS2 sequences with α-proteobacterial GluRS1 and GluRS2 farthest from each other; the ϵ-proteobacterial GluRS2 appears evolutionary far from the rest. Interestingly, GluRS1/GluRS2 of hyperthermophilic bacteria appear at the border of GluRS1/GluRS2 separation.


Evolutionary insights about bacterial GlxRS from whole genome analyses: is GluRS2 a chimera?

Dasgupta S, Basu G - BMC Evol. Biol. (2014)

Phylogeny of bacterial GluRS1 and GluRS2. Phylogenetic tree of bacterial GluRS1 and GluRS2 sequences (listed in Additional file 5) and annotated with bacterial phyla (abbreviations in Table 1). Experimentally determined glutamylation capacity of both GluRS1 and GluRS2 for selected bacterial species (H. pylori, A. ferrooxidans and T. maritima) with the two isoacceptors of tRNAGlu (E1: 34UUC and E2: 34CUC) and tRNAGln (Q1: 34UUG and Q2: 34CUG), are projected in the respective clades, as productive or non-productive (empty/filled symbols). Branch support values < 0.7, calculated using aLRT statistics, are indicated.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC3927822&req=5

Figure 5: Phylogeny of bacterial GluRS1 and GluRS2. Phylogenetic tree of bacterial GluRS1 and GluRS2 sequences (listed in Additional file 5) and annotated with bacterial phyla (abbreviations in Table 1). Experimentally determined glutamylation capacity of both GluRS1 and GluRS2 for selected bacterial species (H. pylori, A. ferrooxidans and T. maritima) with the two isoacceptors of tRNAGlu (E1: 34UUC and E2: 34CUC) and tRNAGln (Q1: 34UUG and Q2: 34CUG), are projected in the respective clades, as productive or non-productive (empty/filled symbols). Branch support values < 0.7, calculated using aLRT statistics, are indicated.
Mentions: In order to further probe the evolutionary relationship between GluRS1 and GluRS2, a phylogenetic tree was constructed, exclusively with GluRS1 and GluRS2 sequences (Additional file 5). The GluRS1/GluRS2 phylogeny (Figure 5) shows a clear division between GluRS1 and GluRS2 sequences with α-proteobacterial GluRS1 and GluRS2 farthest from each other; the ϵ-proteobacterial GluRS2 appears evolutionary far from the rest. Interestingly, GluRS1/GluRS2 of hyperthermophilic bacteria appear at the border of GluRS1/GluRS2 separation.

Bottom Line: Non-functional GluRS2 (as in Thermotoga maritima), on the other hand, was found to contain an anticodon-binding domain appended to a gene-duplicated catalytic domain.Several genomes were found to possess both GluRS2 and GlnRS, even though they share the common function of aminoacylating tRNAGln.The functional annotation of GluRS, without recourse to experiments, performed in this work, demonstrates the inherent and unique advantages of using whole genome over isolated sequence databases.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biophysics, Bose Institute, P-1/12 CIT Scheme VIIM, Kolkata 700054, India. gautam@boseinst.ernet.in.

ABSTRACT

Background: Evolutionary histories of glutamyl-tRNA synthetase (GluRS) and glutaminyl-tRNA synthetase (GlnRS) in bacteria are convoluted. After the divergence of eubacteria and eukarya, bacterial GluRS glutamylated both tRNAGln and tRNAGlu until GlnRS appeared by horizontal gene transfer (HGT) from eukaryotes or a duplicate copy of GluRS (GluRS2) that only glutamylates tRNAGln appeared. The current understanding is based on limited sequence data and not always compatible with available experimental results. In particular, the origin of GluRS2 is poorly understood.

Results: A large database of bacterial GluRS, GlnRS, tRNAGln and the trimeric aminoacyl-tRNA-dependent amidotransferase (gatCAB), constructed from whole genomes by functionally annotating and classifying these enzymes according to their mutual presence and absence in the genome, was analyzed. Phylogenetic analyses showed that the catalytic and the anticodon-binding domains of functional GluRS2 (as in Helicobacter pylori) were independently acquired from evolutionarily distant hosts by HGT. Non-functional GluRS2 (as in Thermotoga maritima), on the other hand, was found to contain an anticodon-binding domain appended to a gene-duplicated catalytic domain. Several genomes were found to possess both GluRS2 and GlnRS, even though they share the common function of aminoacylating tRNAGln. GlnRS was widely distributed among bacterial phyla and although phylogenetic analyses confirmed the origin of most bacterial GlnRS to be through a single HGT from eukarya, many GlnRS sequences also appeared with evolutionarily distant phyla in phylogenetic tree. A GlnRS pseudogene could be identified in Sorangium cellulosum.

Conclusions: Our analysis broadens the current understanding of bacterial GlxRS evolution and highlights the idiosyncratic evolution of GluRS2. Specifically we show that: i) GluRS2 is a chimera of mismatching catalytic and anticodon-binding domains, ii) the appearance of GlnRS and GluRS2 in a single bacterial genome indicating that the evolutionary histories of the two enzymes are distinct, iii) GlnRS is more widespread in bacteria than is believed, iv) bacterial GlnRS appeared both by HGT from eukarya and intra-bacterial HGT, v) presence of GlnRS pseudogene shows that many bacteria could not retain the newly acquired eukaryal GlnRS. The functional annotation of GluRS, without recourse to experiments, performed in this work, demonstrates the inherent and unique advantages of using whole genome over isolated sequence databases.

Show MeSH
Related in: MedlinePlus